Characterization of an amacrine cell type of the mammalian retina immunoreactive for vesicular glutamate transporter 3
Abstract
Immunocytochemical staining of vertical sections through rat, mouse, and macaque monkey retinae with antibodies against the vesicular glutamate transporter vesicular glutamate transporter 3 (vGluT3) showed a sparse population of amacrine cells. The labeled cells had similar appearances in the three species and probably represent homologous types. They were studied in detail in the rat retina. The thin varicose dendrites of vGluT3 amacrine cells formed a convoluted dendritic tree of approximately 100 microm in diameter that was bistratified in the center of the inner plexiform layer. The dendrites of vGluT3 cells were squeezed between the two strata of cholinergic dendrites. The density of vGluT3 cells was measured in retinal wholemounts and increased from 200/mm2 in peripheral retina to 400/mm2 in central retina, accounting for about 1% of all amacrine cells in the rat retina. The vGluT3 cells had a two- to threefold dendritic overlap, and their cell bodies formed a regular mosaic, suggesting they represent a single type of amacrine cell. The vGluT3 amacrine cells expressed glycine and glycine transporter 1 (GlyT1) but not the vesicular glycine transporter (vesicular inhibitory amino acid transporter). They also expressed glutamate; hence, there is the possibility that, comparable to cholinergic amacrine cells, they are "dual transmitter" amacrine cells. The synaptic input of vGluT3 cells was studied by electron microscopy. They received input from bipolar cells at ribbon synapses and from other amacrine cells at conventional synapses. The types of bipolar cells possibly involved with vGluT3 cells were demonstrated by double labeling sections for vGluT3 and the calcium-binding protein CaB5. The axon terminals of type 3 and 5 bipolar cells costratified with vGluT3 dendrites, and it is possible that vGluT3 cells have ON and OFF light responses.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
vGAT is not expressed in vGluT3+ retinal amacrine cells or their axon terminals.
“vGAT is not expressed in vGluT3+ retinal amacrine cells or axon terminals, 102”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [102]
Cites
The Major Cell Populations of the Mouse Retina
Jeon, C.-J., Strettoi, E., & Masland, R. H. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08936.1998 · Cited by 1,429 · see citing works
The Expression of Vesicular Glutamate Transporters Defines Two Classes of Excitatory Synapse
Fremeau, R. T., Troyer, M. D., Pahner, I., Nygaard, G. O., Tran, C. H., Reimer, R. J., Bellocchio, E. E., Fortin, D. L., Storm‐Mathisen, J., & Edwards, R. H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00344-0 · Cited by 1,266 · see citing works
Functional architecture of the mammalian retina
Wässle, H., & Boycott, B. B. (1991) · Physiological Reviews · doi:10.1152/physrev.1991.71.2.447 · Cited by 1,093 · see citing works
Self-citationOrganization of the primate retina: electron microscopy
Dowling, J. E., & Boycott, B. B. (1966) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1966.0086 · Cited by 1,038 · see citing works
Takamori, S., Rhee, J. S., Rosenmund, C., & Jahn, R. (2000) · Nature · doi:10.1038/35025070 · Cited by 862 · see citing works
Uptake of Glutamate into Synaptic Vesicles by an Inorganic Phosphate Transporter
Bellocchio, E. E., Reimer, R. J., Fremeau, R. T., & Edwards, R. H. (2000) · Science · doi:10.1126/science.289.5481.957 · Cited by 795 · see citing works
Feldmeyer, D., Lübke, J., Silver, R. A., & Sakmann, B. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.012959 · Cited by 656 · see citing works
Danysz, W., & Parsons, C. G. (1998) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01382-6 · Cited by 649 · see citing works
A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons
Gras, C., Herzog, E., Bellenchi, G. C., Bernard, V., Ravassard, P., Pohl, M., Gasnier, B., Giros, B., & El Mestikawy, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05442.2002 · Cited by 639 · see citing works
Herzog, É., Bellenchi, G. C., Gras, C., Bernard, V., Ravassard, P., Bedet, C., Gasnier, B., Bruno Giros, A., & Mestikawy, S. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-22-j0001.2001 · Cited by 625 · see citing works
Fremeau, R. T., Burman, J. L., Qureshi, T., Tran, C. H., Proctor, J. M., Johnson, J., Zhang, H., Sulzer, D. L., Copenhagen, D. R., Storm‐Mathisen, J., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.222546799 · Cited by 568 · see citing works
The mosaic of nerve cells in the mammalian retina
Wässle, H., & Riemann, H. J. (1978) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1978.0026 · Cited by 546 · see citing works
Self-citationGlycine transporters are differentially expressed among CNS cells
Zafra, F., Aragón, C., Olivares, L., Danbolt, N. C., Giménez, C., & Storm‐Mathisen, J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03952.1995 · Cited by 521 · see citing works
Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study
Kolb, H., Nelson, R., & Mariani, A. P. (1981) · Vision Research · doi:10.1016/0042-6989(81)90013-4 · Cited by 510 · see citing works
Rod and Cone Pathways in the Inner Plexiform Layer of Cat Retina
Kolb, H., & Famiglietti, E. V. (1974) · Science · doi:10.1126/science.186.4158.47 · Cited by 467 · see citing works
Extreme Diversity among Amacrine Cells: Implications for Function
MacNeil, M. A., & Masland, R. H. (1998) · Neuron · doi:10.1016/s0896-6273(00)80478-x · Cited by 463 · see citing works
A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina
Famiglietti, E. V., & Kolb, H. (1975) · Brain Research · doi:10.1016/0006-8993(75)90983-x · Cited by 456 · see citing works
A Calcium-Dependent Feedback Mechanism Participates in Shaping Single NMDA Miniature EPSCs
Umemiya, M., Chen, N., Raymond, L. A., & Murphy, T. H. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00001.2001 · Cited by 449 · see citing works
Glycine binding primes NMDA receptor internalization
Nong, Y., Huang, Y., Ju, W. H., Kalia, L. V., Ahmadian, G., Wang, Y. T., & Salter, M. W. (2003) · Nature · doi:10.1038/nature01497 · Cited by 427 · see citing works
Kosaka, T., Tauchi, M., & Dahl, J. L. (1988) · Experimental Brain Research · doi:10.1007/bf00247609 · Cited by 417 · see citing works
Schäfer, M. K.-H., Varoqui, H., Defamie, N., Weihe, E., & Erickson, J. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206738200 · Cited by 410 · see citing works
Immunocytochemical identification of cone bipolar cells in the rat retina
Euler, T., & Wässle, H. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903610310 · Cited by 347 · see citing works
Self-citationNeuronal diversity in the retina
Masland, R. H. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00230-0 · Cited by 320 · see citing works
Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases
Sagné, C., Mestikawy, S. E., Isambert, M., Hamon, M., Henry, J., Bruno Giros, A., & Gasnier, B. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01279-9 · Cited by 311 · see citing works
Cholinergic amacrine cells in the rat retina
Voigt, T. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902480103 · Cited by 284 · see citing works
Five Members of a Novel Ca2+-binding Protein (CABP) Subfamily with Similarity to Calmodulin
Haeseleer, F., Sokal, I., Verlinde, C. L. M. J., Erdjument‐Bromage, H., Tempst, P., Pronin, A. N., Benovic, J., Fariss, R. N., & Palczewski, K. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.2.1247 · Cited by 266 · see citing works
Differential expression of three glutamate transporter subtypes in the rat retina
Rauen, T., Rothstein, J. D., & W�ssle, H. (1996) · Cell and Tissue Research · doi:10.1007/s004410050702 · Cited by 249 · see citing works
Self-citationMolecular cloning and functional characterization of human vesicular glutamate transporter 3
Takamori, S., Malherbe, P., Broger, C., & Jahn, R. (2002) · EMBO Reports · doi:10.1093/embo-reports/kvf159 · Cited by 231 · see citing works
Brecha, N., Johnson, D., Peichl, L., & Wässle, H. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.16.6187 · Cited by 225 · cited 1× · see citing works
“An example for such “dual transmitter” cells of the retina are cholinergic amacrine cells, which apparently release acetylcholine and GABA (Brecha et al., 1988; Kosaka et al., 1988; Vaney and Young, 1988; O’Malley and Masland, 1989).”
BackgroundGABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina
Vaney, D. I., & Young, H. M. (1988) · Brain Research · doi:10.1016/0006-8993(88)91366-2 · Cited by 211 · see citing works
Immunocytochemical description of five bipolar cell types of the mouse retina
Haverkamp, S., Ghosh, K. K., Hirano, A. A., & Wässle, H. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10491 · Cited by 209 · see citing works
Self-citationGlutamate Responses of Bipolar Cells in a Slice Preparation of the Rat Retina
Euler, T., Schneider, H., & Wässle, H. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-09-02934.1996 · Cited by 207 · see citing works
Self-citationSassoé‐Pognetto, M., Wässle, H., & Grünert, U. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-08-05131.1994 · Cited by 204 · see citing works
Self-citationPourcho, R. G., & Goebel, D. J. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902330406 · Cited by 201 · see citing works
Johnson, J., Tian, N., Caywood, M. S., Reimer, R. J., Edwards, R. H., & Copenhagen, D. R. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-02-00518.2003 · Cited by 197 · see citing works
Wäussle, H., Grüunert, U., & Röhrenbeck, J. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903320403 · Cited by 190 · see citing works
Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat
Krout, K. E., & Loewy, A. D. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000814)424:1 · Cited by 180 · see citing works
Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron
O'Malley, D. M., & Masland, R. H. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.9.3414 · Cited by 150 · see citing works
Neurotransmitter Coupling through Gap Junctions in the Retina
Vaney, D. I., Nelson, J. C., & Pow, D. V. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10594.1998 · Cited by 149 · see citing works
Molecular Phenotyping of Retinal Ganglion Cells
Marc, R. E., & Jones, B. W. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-00413.2002 · Cited by 149 · see citing works
Functional Organization of Cone Bipolar Cells in the Rat Retina
Hartveit, E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.4.1716 · Cited by 133 · see citing works
G protein subunit Gγ13 is coexpressed with Gαo, Gβ3, and Gβ4 in retinal ON bipolar cells
Huang, L., Max, M., Margolskee, R. F., Su, H., Masland, R. H., & Euler, T. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10396 · Cited by 126 · see citing works
Large-scale morophological survey of rat retinal ganglion cells
Sun, W., LI, N., & He, S. (2002) · Visual Neuroscience · doi:10.1017/s0952523802194107 · Cited by 121 · see citing works
The number of unidentified amacrine cells in the mammalian retina
Strettoi, E., & Masland, R. H. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.25.14906 · Cited by 115 · see citing works
Amino acid neurochemistry of the vertebrate retina
Kalloniatis, M. (1999) · Progress in Retinal and Eye Research · doi:10.1016/s1350-9462(98)00036-6 · Cited by 112 · see citing works
The immunocytochemical detection of amino-acid neurotransmitters in paraformaldehyde-fixed tissues
Pow, D. V., Wright, L. L., & Vaney, D. I. (1995) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(94)00113-u · Cited by 107 · see citing works
Vesicular γ‐aminobutyric acid transporter expression in amacrine and horizontal cells
Cueva, J. G., Haverkamp, S., Reimer, R. J., Edwards, R. H., Wässle, H., & Brecha, N. C. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10166 · Cited by 84 · see citing works
Self-citationAmino acids and their transporters in the retina
Pow, D. V. (2001) · Neurochemistry International · doi:10.1016/s0197-0186(00)00114-5 · Cited by 84 · see citing works
Karchewski, L. A., Kim, F. A., Johnston, J. M., McKnight, R. M., & Verge, V. M. K. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991018)413:2 · Cited by 81 · see citing works
Fujiyama, F., Hioki, H., Tomioka, R., Taki, K., Tamamaki, N., Nomura, S., Okamoto, K., & Kaneko, T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10848 · Cited by 81 · see citing works
Transport-Mediated Synapses in the Retina
Schwartz, E. A. (2002) · Physiological Reviews · doi:10.1152/physrev.00010.2002 · Cited by 56 · see citing works
The DAPI-3 amacrine cells of the rabbit retina
Wright, L. L., Macqueen, C. L., Elston, G. N., Young, H. M., Pow, D. V., & Vaney, D. I. (1997) · Visual Neuroscience · doi:10.1017/s0952523800012141 · Cited by 51 · see citing works
Kim, I., Lee, E. J., Oh, S.-J., et al. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10359 · Cited by 45 · see citing works
Immunohistochemical localization of caffeine-induced c-Fos protein expression in the rat brain
Bennett, H. J., & Semba, K. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19981109)401:1 · Cited by 41 · see citing works
Light-and electron-microscopic studies of the somatostatin-immunoreactive plexus in the cat retina
Chun, M., Brecha, N. C., & W�ssle, H. (1992) · Cell and Tissue Research · doi:10.1007/bf00318691 · Cited by 17 · see citing works
Self-citationThe fountain amacrine cells of the rabbit retina
Wright, L. L., & Vaney, D. I. (1999) · Visual Neuroscience · doi:10.1017/s0952523899166148 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · see citing works
Lee, S., Zhang, Y., Chen, M., & Zhou, Z. J. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.023 · Cited by 101 · see citing works
Tien, N.-W., Kim, T., & Kerschensteiner, D. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.025 · Cited by 67 · see citing works
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
- Authors
- Haverkamp, S., & Wässle, H.
- Affiliations
- Max Planck Institute for Brain Research (DE)
- Corresponding author
- Wässle, Heinz
- ORCID
- Haverkamp, Silke
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2003-11-26
- Volume
- 468
- Issue
- 2
- Pages
- 251-263
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1965956049
- Cited by
- 110
- References
- 56
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 2 · 2023: 8 · 2022: 4 · 2021: 3 · 2020: 11 · 2019: 3 · 2018: 2 · 2017: 12 · 2016: 5 · 2015: 5 · 2014: 4 · 2013: 3 · 2012: 3
- FWCI
- 1.73
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (SFB 269/B4)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
- Keywords
- amacrine cells, VGLUT3, retina, inner plexiform layer, dendritic morphology, glycine transporter 1, cholinergic amacrine cells, bipolar cells, ribbon synapses, synaptic input, species comparison
- MeSH terms
- Animals, Immunohistochemistry, Macaca fascicularis, Mice, Inbred C57BL, Rabbits, Retina, Rats, Wistar, Amacrine Cells, Amino Acid Transport Systems, Acidic, Vesicular Glutamate Transport Proteins, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review